Besides stomata, the photosynthetic CO2 pathway also involves the transport of CO2 from the sub-stomatal air spaces inside to the carboxylation sites in the chloroplast stroma, where Rubisco is located. This pathway is far to be a simple and direct way, formed by series of consecutive barriers that the CO2 should cross to be finally assimilated in photosynthesis, known as the mesophyll conductance (gm). Therefore, the gm reflects the pathway through different air, water and biophysical barriers within the leaf tissues and cell structures. Currently, it is known that gm can impose the same level of limitation (or even higher depending of the conditions) to photosynthesis than the wider known stomata or biochemistry. In this mini-review, we are focused on each of the gm determinants to summarize the current knowledge on the mechanisms driving gm from anatomical to metabolic and biochemical perspectives. Special attention deserve the latest studies demonstrating the importance of the molecular mechanisms driving anatomical traits as cell wall and the chloroplast surface exposed to the mesophyll airspaces (Sc/S) that significantly constrain gm. However, even considering these recent discoveries, still is poorly understood the mechanisms about signaling pathways linking the environment a/biotic stressors with gm responses. Thus, considering the main role of gm as a major driver of the CO2 availability at the carboxylation sites, future studies into these aspects will help us to understand photosynthesis responses in a global change framework.

Photosynthesis: a three-team ‘match’

In C3 plants, three major physiological and biochemical processes drive photosynthesis: the stomatal conductance (gs), the mesophyll conductance (gm) and the biochemistry lead by the Rubisco enzyme. Besides stomata, the photosynthetic CO2 pathway also involves the diffusion of CO2 from the sub-stomatal air spaces inside to the carboxylation sites in the chloroplast stroma (where Rubisco is located). This pathway is far from being a simple and direct way, consisting of a complex of consecutive barriers up to the stroma carboxylation sites, when considered jointly is referred as the internal or mesophyll conductance [1]. Therefore, the gm reflects the pathway through different air, water and biophysical barriers, which we discuss in more detail here.

Mesophyll conductance is usually obtained by three different methodologies, combining gas exchange measurements with either online carbon and oxygen isotope discrimination [2–5] or chlorophyll fluorescence [6,7]. But a combination of both techniques is the most used [8–10]) and also by the curve-fitting method employing AN-Ci curves [11–13]. In earlier works, gm was considered infinite and thus not a limiting factor of photosynthesis, so gs and photo-biochemistry were considered the main players driving the photosynthesis ‘game' (Figure 1A). In this simplified vision, only one factor would be the most limiting for photosynthesis under a certain condition and improving such a single factor should lead to increased photosynthesis. Additionally, under this assumption Ci should be equal to Cc, but it is now well accepted that gm can impose significant limitations to photosynthesis (in the same order of magnitude or even more than gs) depending on the plants and the prevailing environmental conditions, implying that Cc will be considerable minor than Ci [1,14–16]. It is important to note that the achieved Cc is not just depending of the CO2 flow within the leaf, but also to the consumption velocity of the CO2 by the Rubisco integrated to the whole photosynthetic metabolism (i.e. the electron transport rate (ETR) in the thylakoids, the maximum carboxylation rate by Rubisco (Vc,max), and the RuBP regeneration in the Calvin cycle) [17]. Thus, the photosynthesis game is not just a matter of two, but three players interacting (Figure 1B). In this context, maximal potential photosynthesis can be limited by one, two or even three of them (if they are co-limiting in a balanced manner). Indeed, it was recently reported that angiosperms showed the largest photosynthetic rates as compared with other phylogenetic plant groups with a co-balanced limitation between these three factors [16].

Photosynthesis: a three-team ‘match’.

Figure 1.
Photosynthesis: a three-team ‘match’.

(A) Photosynthesis was traditionally considered as a balance between the stomatal conductance (gs) regulating the CO2 diffusion (i.e. the ‘supply’) and the pool of photo-biochemistry reactions, here represented as a classical soccer match game with two players: ‘gs team' versus the ‘photo-biochemistry team'. Like in a soccer game, only three results are possible: (1) one ‘wins’ (i.e. limits photosynthesis the most), (2) the other does, or (3) the two ‘tie’ (i.e. co-limited photosynthesis). (B) However, mesophyll conductance (gm) can impose significant limitations to photosynthesis (lm), of the same order of magnitude than the limitations imposed by the stomata (ls) and the photo-biochemistry (lb), which is illustrated as a much complex football match being played by three teams simultaneously, i.e. largely increasing the number of potential ‘results’ (i.e. combinations of main limiting factors).

Figure 1.
Photosynthesis: a three-team ‘match’.

(A) Photosynthesis was traditionally considered as a balance between the stomatal conductance (gs) regulating the CO2 diffusion (i.e. the ‘supply’) and the pool of photo-biochemistry reactions, here represented as a classical soccer match game with two players: ‘gs team' versus the ‘photo-biochemistry team'. Like in a soccer game, only three results are possible: (1) one ‘wins’ (i.e. limits photosynthesis the most), (2) the other does, or (3) the two ‘tie’ (i.e. co-limited photosynthesis). (B) However, mesophyll conductance (gm) can impose significant limitations to photosynthesis (lm), of the same order of magnitude than the limitations imposed by the stomata (ls) and the photo-biochemistry (lb), which is illustrated as a much complex football match being played by three teams simultaneously, i.e. largely increasing the number of potential ‘results’ (i.e. combinations of main limiting factors).

In this mini-review, we are focused on the latest advances about the mechanisms driving gm from anatomical to metabolic and biochemical perspectives. Considering the main role of gm as a major driver of the CO2 availability at the carboxylation sites, future studies into these aspects will help us to understand photosynthesis responses in a changing environment. If the reader is also interested into the mechanisms driving the role of gs and Rubisco carboxylation we can suggest several recent works and reviews with the latest insights [18–22].

Mesophyll diffusion conductance

General features

If stomatal conductance can be viewed as the degree of opening of a single door from the atmosphere to inside the leaves, mesophyll conductance can be viewed as an integrative degree of opening of the multiple corridors allowing CO2 to move from the sub-stomatal cavity to the site of carboxylation inside chloroplasts’ stroma. This complex pathway (Figure 2) includes a gas phase component (i.e. the so-called intercellular air spaces conductance, gias), several aqueous components (cell wall conductance, gcw; cytosol conductance, gcyt; and stroma conductance, gst) and two lipid–protein components (plasma membrane conductance, gpl, and chloroplast membrane conductance, gcm). While these components can potentially vary independently each other, most current methods to estimate internal diffusion only permit and integrative estimate of the diffusion conductance of the whole pathway, i.e. the so-called mesophyll conductance (gm). For this reason, in the next sections we will mostly refer to gm only, yet indicating which of the partial conductance is mostly involved whenever this information is available. However, it is worth noting that novel advances are questioning this approach to CO2 diffusion due to the potential artifacts in gm when considering the re-assimilation of the CO2 produced during photorespiration [23]. New reaction-diffusion and two-resistance models that consider all processes affecting Cc may provide more accurate estimations of gm and insight of the additional structural features that affect it, such as mitochondria positioning and the 3-D structure of the mesophyll [24–27].

The gates and leaf corridors for photosynthesis.

Figure 2.
The gates and leaf corridors for photosynthesis.

Both stomatal and mesophyll conductance (gs and gm, respectively) are the CO2 diffusion pathways from the stomata guard cells into the mesophyll tissues where photosynthesis takes place inside chloroplasts. From the atmosphere the CO2 (Ca) diffuses through the guard cells of stomata (gs) into the sub-stomatal cavities at a certain concentration (Ci). From the sub-stomatal cavities the CO2 crosses a series of biophysical barriers composed by air, water and lipid elements that are reflected by gm. The internal gas-phase diffusion (gias) is the CO2 pathway from the sub-stomatal cavities to the outer surface of the mesophyll cell walls and is determined by the effective mesophyll thickness, porosity and tortuosity. From this point the CO2 diffuses through the liquid-phase diffusion (gliq) that basically comprises the cell structure barriers up to the carboxylation sites in the chloroplast stroma. This phase consists of the conductance through the cell wall (gcw), the plasma membrane (gpl), the cytoplasm (gcyt), chloroplast membrane (gcm) and the chloroplast stroma (gst) up to the carboxylation sites (Cc) where Rubisco is located to perform the photosynthetical process.

Figure 2.
The gates and leaf corridors for photosynthesis.

Both stomatal and mesophyll conductance (gs and gm, respectively) are the CO2 diffusion pathways from the stomata guard cells into the mesophyll tissues where photosynthesis takes place inside chloroplasts. From the atmosphere the CO2 (Ca) diffuses through the guard cells of stomata (gs) into the sub-stomatal cavities at a certain concentration (Ci). From the sub-stomatal cavities the CO2 crosses a series of biophysical barriers composed by air, water and lipid elements that are reflected by gm. The internal gas-phase diffusion (gias) is the CO2 pathway from the sub-stomatal cavities to the outer surface of the mesophyll cell walls and is determined by the effective mesophyll thickness, porosity and tortuosity. From this point the CO2 diffuses through the liquid-phase diffusion (gliq) that basically comprises the cell structure barriers up to the carboxylation sites in the chloroplast stroma. This phase consists of the conductance through the cell wall (gcw), the plasma membrane (gpl), the cytoplasm (gcyt), chloroplast membrane (gcm) and the chloroplast stroma (gst) up to the carboxylation sites (Cc) where Rubisco is located to perform the photosynthetical process.

The anatomical determinants of mesophyll diffusion conductance

Both maximum values of gm and gs can be achieved under the same physiological and environmental non-stress conditions [1]. However, gm is a much more complex photosynthetic trait, since it results from the total CO2 diffusion efficiency of each of the different gas- and liquid-phase components comprised between the intercellular airspaces and the carboxylation sites [28,29]. In turn, the conductance to CO2 diffusion of each component is determined by several properties: (1) the CO2 diffusivity of each phase (e.g. diffusion in the liquid phase is by four orders of magnitude slower than in the gas phase), (2) the diffusion path length, being the shortest pathway the most effective one, and (3) the effective porosity. This last one, is also determined by (i) the structure and composition of the component, which sets the tortuosity and the porosity (effective porosity = tortuosity/porosity), and (ii) the presence of mediators like aquaporins and carbonic anhydrases (CAs) [28,30–32], discussed in more detail in next section. Moreover, the liquid-phase conductance is escalated by both mesophyll and chloroplast surface areas exposed to intercellular airspaces per unit of leaf area (Sm/S and Sc/S, respectively), which allow to increase the area for CO2 dissolution and to decrease the effective pathway for CO2 diffusion [29]. The cytosol comprised between the plasma and chloroplast membranes only plays a minor role in limiting gm, as chloroplasts tend to be closely lined up with cell walls (CWs) under high light conditions to reduce the CO2 effective pathway [28,29,32]. However, cases have been reported in which chloroplasts detach from the plasma membrane, which leads to a decrease in gm [33].

Consequently, in order to maximize gm efficiency, leaves need to reduce the diffusion path length (anatomically determined) and increase both Sc/S and the effective porosity of each cellular component of gm [28,29]. Sc/S and gm are tightly correlated across species, genotypes and treatments [9,34–38]. Recent efforts have attempted to manipulate the mesophyll properties to maximize Sc/S and thus consequently increasing the photosynthetic capacity [39]. Besides Sc/S, other important traits appear determining gm, but, how can we know which are these other traits? For that, analytical 1-D and 3-D models of gm allow dissecting the mesophyll CO2 diffusion pathway by modeling the partial limitation imposed by each pathway component on gm [25,31,35,37,40–42]. Interestingly, these models have revealed that usually the main constraints on gm reside in the CW and in the chloroplast stroma.

Cell wall, the first component of the liquid phase, can impose up to 90% of the gm limitations [38] and a recent data compilation of CW thickness (Tcw) has been measured in hundreds of species [16]. It is tightly correlated with gm, describing a linear negative function when accounting for angiosperms and ferns [29,36,37,39], which turns into an exponential decay function when including the thick-walled gymnosperms and bryophytes [38,43]. The other main physical limitation is the chloroplast stroma, where the carbon fixation by Rubisco occurs [28,44]. Due to the low affinity of Rubisco for CO2, it is suggested that the resistance for CO2 diffusion in the stroma decreases with the Rubisco content per unit Sc/S (i.e. the thinner and elongated the chloroplast (thus, exposing a higher surface of the chloroplast to the mesophyll airspaces) the better photosynthesis increase) [29]. Thus, chloroplast stroma would be the major limitation to gm in species with high photosynthetic capacity and very thin CWs [35,45], or in species that present very thick chloroplasts as is the case of some lycophytes [37,38]. Nevertheless, as it happens with CWs, the effective diffusivity (or porosity) of the chloroplast stroma is still unknown. Keeping the focus inside the cell, the role of intercellular space on setting gm is presumably smaller. Due to its high diffusivity is normally considered to be the easiest component to go through, reason by which some studies neglect it [26,28,30]. However, mesophyll porosity can vary greatly between species from 3 to 73% [26,46] and, in species with thick leaves and especially dense mesophyll tissues, the tortuosity, the connectivity and the lateral path lengthening of this component can be especially affected, causing important intercellular space limitations to gm [26,47].

Last but not least, in the last few decades some studies have reported that cytosol receives, apart from the CO2 flux from the plasma membrane, a flux of CO2 photorespired by mitochondria [30] and released by chloroplasts [48]. Although the presumably contribution of this photorespired CO2 in the general CO2 flux would depend on the arrangement of mitochondria and chloroplasts, traditional photosynthesis models assume a tight arrangement of chloroplasts closely lined up to the plasma membrane, being mitochondria located behind chloroplasts. So, CO2 released by mitochondria into the cytosol could diffuse to other sinks than chloroplasts and, consequently, it would convert artifactual gm estimations since these wouldn't be represented in the sum of physical resistances [25,27,41].

Mesophyll conductance responses to the environment

Mesophyll conductance is nowadays widely recognized as a determinant of photosynthesis changes in response to abiotic environmental variations from the short- to the long-term [1,32]. At the short-term studies (i.e. seconds to minutes), gm has been established to respond, although neither in all species nor under all conditions, to CO2 [49–53], light [49,50,52–54], temperature [14,40,55–59], drought [60–62] and salinity [13,63–65]. However, these short-term responses have to be taken with caution, as in most cases there is no clear evidence of the mechanistic basis regulating those gm changes [28,38,59,66] and several potential artifacts or problems in the calculations of the models have been detected (e.g. type-II errors, effects of photorespired CO2, intra-leaf light gradients) [25,27,30,67,68]. On the other hand, at long-term studies more evidences of gm regulations have been obtained in response to CO2, light, temperature, ozone, water stress and/or nutrients, including anatomical variations [31,57,69–73], changes in aquaporin (AQPs) as well as CAs expression and activity [74]. The mechanisms by which environmental conditions are sensed and signaled to induce modifications of gm are still poorly understood and an important matter of debate [13,14,59,75]. As with gs, hydraulic signaling has been hypothesized — but not firmly demonstrated — because water and CO2 share a significant fraction of their respective pathways inside leaves [32,58,76,77].

To cope with the environmental stressors, abscisic acid (ABA) is the main abiotic stress-related phytohormone in seed plants [78], which also has been shown to induce modifications of gm [51,79]. However, in these studies it could not be discerned whether the effect of ABA on gm was direct or indirect through modulating gs nor both conductance co-regulation through an independent mechanism. Recently, uncoupled responses between gs and gm to ABA have been described in Arabidopsis mutant lines lacking OST1 and SAC1, suggesting a direct effect of ABA on gm through a pathway independent of that for gs [75]. Nevertheless, more studies are needed to understand the signaling pathways linking the environment a/biotic stressors with gm change responses.

Biochemical regulation of the mesophyll diffusion conductance

The biochemical mechanisms driving gm still remain mostly unknown, however in the last years this is becoming an emergent and exciting topic within the scientific community. Several of the different traits previously mentioned are driven and/or modified by known metabolic routes, but almost never explored in relation to gm.

We stated previously that CW thickness (Tcw) is one of the most important anatomical parameters related to gm. However, there are no direct measurements of the effective porosity of CWs to CO2 diffusion for terrestrial plants, in which only some approximations or assumptions about its relationship with Tcw are available [29,31,35,80]. It is known that CW pores are an order of magnitude larger than CO2 molecules [28], for which how Tcw affects CO2 diffusion still is unclear. Otherwise, it could be not only the thickness of the CW what matters but other non-anatomical factors could determine gm. In particular, how both the way CW structure and its biochemical composition could affect structural features (such as porosity and tortuosity) and/or provoke different physico-chemical interactions in the CO2 diffusion pathway deserves further exploration. CWs are not stationary structures within the tissues; in which continuously take place-remodeling processes in response to environmental and physiological stimuli by abiotic/biotic factors [81,82]. Indirect evidences from multi-species meta-analysis modeling showed exclusive associations between gm with metabolites mostly related with CW metabolism, such as xylose, arabinose, hydroxybenzoate and gluconate [83]. More recently, different authors have reported how changes in CW composition (specifically hemicelluloses and pectins) can affect gm. For example, rice mutants with defective production of mixed-linkage glucan showed reductions in gm [84]. Under salinity and drought stress, leaves tobacco plants displayed modifications in the CW composition (mainly changes in pectins and the ratio pectins/hemicelluloses) associated with gm functionality [85]. In turn, it was related with the apoplast redox state and its antioxidant enzymatic activity, such as peroxidases, so altogether driving CW composition changes [85]. These novel studies offer additional information that may enable us to understand the biochemical and molecular mechanisms driving gm and its responses to abiotic stressors.

Besides CWs within the liquid phase, an additional ‘barrier' of lipid nature consists of both cell and chloroplast membranes. Still is a matter of debate their permeability to the CO2 because the proposed current values differ in orders of magnitude [1]. Even more uncertainties can be expected considering that lipid and protein membrane composition can be strongly remodeled in response to the environment [86,87]. Under stress conditions, membrane antioxidant lipophilic composition (carotenoids and tocopherols) can be altered [88–90], as well as the integral transmembrane proteins activity [91,92]. Unfortunately, how membrane composition affects the direct permeation coefficient still remains unexplored in the field.

On the other hand, AQPs are channel proteins that can facilitate CO2 diffusion into the cells [93,94] and its activity were tested in vivo showing higher gm in AQPs overexpressing plants [95–98]. Indeed, those increases were lately related with higher productivity in rice plants overexpressing the Oryza sativa Plasma membrane Intrinsic Protein 1;2 (abbreviated as PIP1;2) with increased gm by 150% compared with the wild type [99]. Interestingly, in general gm increases concomitantly co-ordinates with increases in gs, thus increasing AN but not the WUEi [17]. In addition, employing tobacco NtAQP1 RNA interference (RNAi) plants it was shown that CO2 permeability was reduced by 90% in chloroplast envelopes, however just 10% in the cell membrane. Interestingly, these reductions just have a slight effect in gm (ca. 20%) [97]. Although there is an important uncertainty regarding the permeability of the lipid membranes, AQPs presumably constitute a compensatory mechanism to ensure CO2 supply into the stroma.

Another family of proteins related to gm, the carbonic anhydrases (CAs, located mostly in the stroma but also in mitochondria, cytosol and plasma membrane) are zinc metalloenzymes that catalyze the interconversion of CO2 into HCO3 with higher efficiency [100]. Despite earlier experiments overexpressing CAs showed little improvements in gm and AN [101,102], recent studies have shown evidence of their potential role in gm [74,103]. Further studies in a latitudinal genotype transect in Populus trichocarpa reported that northern genotypes showed higher AN relating positively gm with their elevated CAs activity [104]. Altogether, the role of CAs in gm in C3 species is still poorly understood, most probably because of the redundant functions of CAs, their multiple cell locations and roles in any reaction that implies CO2 or HCO3 [17,105].

Conclusion

If the stomata are considered the gates of photosynthesis, there is no doubt that mesophyll conductance can be considered the final corridors. However, its complex nature still avoids to fully understanding the main mechanisms driving its responses. Here, we reviewed the most important gm determinants to summarize the current knowledge of the mechanisms driving it from anatomical to metabolic and biochemical perspectives. In accordance, gas, liquid and lipid barriers determine gm, in turn all of them can be affected by responses to environmental factors (mainly, light, CO2 concentration and water availability). For this reason, more studies unraveling and integrating the knowledge from anatomical to metabolomic and biochemical determinants of gm is needed. This information will be essential to address crop improvement on maximal photosynthesis capacity and WUE in the global change scenario.

Perspectives

  • Importance of the field: Mesophyll conductance (gm) is a major actor driving photosynthesis and water use efficiency (WUE). It describes the CO2 pathway from the sub-stomatal cavities to the Rubisco carboxylation sites in the chloroplast stroma of the mesophyll cells. Its importance relies on the fact that gm can limit photosynthesis as much as stomatal conductance and the photobiochemistry.

  • Summary of the current thinking: Besides its well-recognized importance, the large complexity of gm has limited the knowledge acquisition about its mechanistic basis. While the CO2 pathway through stomatal cavities is simple and straight; across the mesophyll CO2 shouldcross a series of consecutive biophysical barriers through leaf tissues and cell structures diffusing in different media (air, lipids, and aqueous phases). Therefore, understanding the main molecular mechanisms driving changes in the relevant anatomical traits affecting gm is currently a major research priority.

  • Future directions: More research efforts are needed to understand the mechanisms driving gm (and thus photosynthesis) responses to both abiotic and biotic factors. Any of the biophysical barriers that constraints gm can be affected by these factors (light, CO2 concentration, water availability…) in a complex manner and at different time scales. Thus, studies integrating different scales to attempt deciphering the molecular mechanisms from metabolism to physiology are needed. Moreover, this knowledge will help designing new crop breeding strategies to maximize photosynthesis and WUE in the global change scenario.

Competing Interests

The authors declare that there are no competing interests associated with the manuscript.

Funding

J.F. and J.G. want to thank the financial support from the Spanish Ministry of Science and Technology, Project EREMITA, [PGC2018-093824-B-C41]. A.N.N., W.L.A. and D.M.D. are also grateful for the financial support from National Council for Scientific and Technological Development (CNPq-Brazil, Grant 402511/2016-6 and Grant 428192/2018-1), and the FAPEMIG (Foundation for Research Assistance of the Minas Gerais State, Brazil, Grant RED-00053-16), and as well by their research fellowships funded by the same institution. M.N. thanks his predoctoral fellowship BES-2015–072578 from the Spanish Ministry of Science and co-financed by the European Social Fund. M.M. thanks her postdoctoral fellowship FJCI-2016-31007 (‘Juan de la Cierva-Formación’ program) co-funded by the Spanish Ministry of Science, Innovation and Universities, the State Research Agency and the University of the Balearic Islands.

Author Contribution

J.G. and J.F. conceived and designed the idea of this mini-review. J.G., D.M.D. and J.F. wrote the first draft of the paper with subsequent inputs from all co-authors. M.N., M.M. and J.F. developed the figures and dataset compilation.

Acknowledgements

We thank Belén Escutia, Universitat de les Illes Balears, for her collaboration in designing the Figures 1 and 2.

Abbreviations

     
  • ABA

    abscisic acid

  •  
  • AN

    net photosynthesis rate

  •  
  • AQPs

    aquaporins

  •  
  • CAs

    carbonic anhydrases

  •  
  • Cc

    chloroplast CO2 concentration

  •  
  • Ci

    intercellular CO2 concentration

  •  
  • CO2

    carbon dioxide

  •  
  • CW

    cell wall

  •  
  • ETR

    electron transport rate

  •  
  • gcm

    chloroplast membrane conductance

  •  
  • gcw

    cell wall conductance

  •  
  • gcyt

    cytoplasm conductance

  •  
  • gias

    gas-phase diffusion conductance

  •  
  • gm

    mesophyll conductance

  •  
  • gpm

    plasma membrane conductance

  •  
  • gs

    stomatal conductance

  •  
  • gst

    chloroplast stroma conductance

  •  
  • Rubisco

    Ribulose-1,5-bisphosphate carboxylase/oxigenase

  •  
  • Sc/S

    chloroplast surface areas exposed to intercellular airspaces per unit of leaf area

  •  
  • Sm/S

    mesophyll surface areas exposed to intercellular airspaces per unit of leaf area

  •  
  • Vc,max

    the maximum carboxylation rate by Rubisco

  •  
  • WUE

    water use efficiency

References

References
1
Flexas
,
J.
,
Barbour
,
M.M.
,
Brendel
,
O.
,
Cabrera
,
H.M.
,
Carriquí
,
M.
,
Díaz-Espejo
,
A.
et al (
2012
)
Mesophyll diffusion conductance to CO2 : an unappreciated central player in photosynthesis
.
Plant Sci.
193–194
,
70
84
2
Farquhar
,
G.D.
,
von Caemmerer
,
S.
and
Berry
,
J.A.
(
1980
)
A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species
.
Planta
149
,
78
90
3
Field
,
C.
,
Berry
,
J.A.
and
Mooney
,
H.A.
(
1982
)
A portable system for measuring carbon dioxide and water vapour exchanges of leaves
.
Plant Cell Environ.
5
,
179
186
4
Evans
,
J.R.
,
Sharkey
,
T.D.
,
Berry
,
J.A.
and
Farquhar
,
G.D.
(
1986
)
Carbon isotope discrimination measured concurrently with gas exchange to investigate CO2 diffusion in leaves of higher plants
.
Aust. J. Plant Physiol.
13
,
281
292
5
Barbour
,
M.M.
,
Evans
,
J.R.
,
Simonin
,
K.A.
and
von Caemmerer
,
S.
(
2016
)
Online CO2 and H2O oxygen isotope fractionation allows estimation of mesophyll conductance in C4 plants, and reveals that mesophyll conductance decreases as leaves age in both C4 and C3 plants
.
New Phytol.
210
,
875
889
6
Harley
,
P.C.
,
Loreto
,
F.
,
Di Marco
,
G.
and
Sharkey
,
T.D.
(
1992
)
Theoretical considerations when estimating the mesophyll conductance to CO2 flux by analysis of the response of photosynthesis to CO2
.
Plant Physiol.
98
,
1429
1436
7
Laisk
,
A.
,
Oja
,
V.
,
Rasulov
,
B.
,
Rämma
,
H.
,
Eichelmann
,
H.
,
Kasparova
,
I.
et al (
2002
)
A computer-operated routine of gas exchange and optical measurements to diagnose photosynthetic apparatus in leaves
.
Plant Cell Environ.
25
,
923
943
8
Pons
,
T.L.
,
Flexas
,
J.
,
Von Caemmerer
,
S.
,
Evans
,
J.R.
,
Genty
,
B.
,
Ribas-Carbó
,
M.
et al (
2009
)
Estimating mesophyll conductance to CO2: methodology, potential errors, and recommendations
.
J. Exp. Bot.
60
,
2217
2234
9
Peguero-Pina
,
J.J.
,
Sisó
,
S.
,
Flexas
,
J.
,
Galmés
,
J.
,
García-Nogales
,
A.
,
Niinemets
,
Ü.
et al (
2017
)
Cell-level anatomical characteristics explain high mesophyll conductance and photosynthetic capacity in sclerophyllous Mediterranean oaks
.
New Phytol.
214
,
585
596
10
Xie
,
K.
,
Lu
,
Z.
,
Pan
,
Y.
,
Gao
,
L.
,
Hu
,
P.
,
Wang
,
M.
et al (
2019
)
Leaf photosynthesis is mediated by the coordination of nitrogen and potassium: the importance of anatomical-determined mesophyll conductance to CO2 and carboxylation capacity
.
Plant Sci.
290
,
110267
11
Ethier
,
G.J.
and
Livingston
,
N.J.
(
2004
)
On the need to incorporate sensitivity to CO2 transfer conductance into the Farquhar – von Caemmerer – Berry leaf photosynthesis model
.
Plant Cell Environ.
27
,
137
153
12
Sharkey
,
T.D.
,
Bernacchi
,
C.J.
,
Farquhar
,
G.D.
and
Singsaas
,
E.L.
(
2007
)
Fitting photosynthetic carbon dioxide response curves for C3 leaves
.
Plant Cell Environ.
30
,
1035
1040
13
Qiu
,
R.J.
and
Katul
,
G.
(
2019
)
Maximizing leaf carbon gain in varying saline conditions: an optimization model with dynamic mesophyll conductance
.
Plant J.
101
,
543
554
14
Flexas
,
J.
,
Ribas-Carbó
,
M.
,
Díaz-Espejo
,
A.
,
Galmés
,
J.
and
Medrano
,
H.
(
2008
)
Mesophyll conductance to CO2: current knowledge and future prospects
.
Plant Cell Environ.
31
,
602
621
15
Nadal
,
M.
and
Flexas
,
J.
(
2019
)
Variation in photosynthetic characteristics with growth form in a water-limited scenario: implications for assimilation rates and water use efficiency in crops
.
Agric. Water Manag.
216
,
457
472
16
Gago
,
J.
,
Carriquí
,
M.
,
Nadal
,
M.
,
Clemente-Moreno
,
M.J.
,
Coopman
,
R.E.
,
Fernie
,
A.R.
et al (
2019
)
Photosynthesis optimized across land plant phylogeny
.
Trends Plant Sci.
24
,
947
958
17
Flexas
,
J.
,
Díaz-Espejo
,
A.
,
Conesa
,
M.A.
,
Coopman
,
R.E.
,
Douthe
,
C.
,
Gago
,
J.
et al (
2016
)
Mesophyll conductance to CO2 and Rubisco as targets for improving intrinsic water use efficiency in C3 plants
.
Plant Cell Environ.
39
,
965
982
18
Tcherkez
,
G.
(
2013
)
Modelling the reaction mechanism of ribulose-1,5-bisphosphate carboxylase/oxygenase and consequences for kinetic parameters
.
Plant Cell Environ.
36
,
1586
1596
19
Assmann
,
S.M.
and
Jegla
,
T.
(
2016
)
Guard cell sensory systems: recent insights on stomatal responses to light, abscisic acid, and CO2
.
Curr. Opin. Plant Biol.
33
,
157
167
20
Brodribb
,
T.J.
and
McAdam
,
S.A.M.
(
2017
)
Evolution of the stomatal regulation of plant water content
.
Plant Physiol.
174
,
639
649
21
Deans
,
R.M.
,
Brodribb
,
T.J.
,
Busch
,
F.A.
and
Farquhar
,
G.D.
(
2019
)
Plant water-use strategy mediates stomatal effects on the light induction of photosynthesis
.
New Phytol.
222
,
382
395
22
Galmés
,
J.
,
Capó-Bauçà
,
S.
,
Niinemets
,
Ü.
and
Iñiguez
,
C.
(
2019
)
Potential improvement of photosynthetic CO2 assimilation in crops by exploiting the natural variation in the temperature response of Rubisco catalytic traits
.
Curr. Opin. Plant Biol.
49
,
60
67
23
Berghuijs
,
H.N.C.
,
Yin
,
X.
,
Ho
,
Q.T.
,
Driever
,
S.M.
,
Retta
,
M.A.
,
Nicolaï
,
B.M.
et al (
2016
)
Mesophyll conductance and reaction-diffusion models for CO2 transport in C3 leaves; needs, opportunities and challenges
.
Plant Sci.
252
,
62
75
24
Ho
,
Q.T.
,
Berghuijs
,
H.N.C.
,
Watté
,
R.
,
Verboven
,
P.
,
Herremans
,
E.
,
Yin
,
X.
et al (
2016
)
Three-dimensional microscale modelling of CO2 transport and light propagation in tomato leaves enlightens photosynthesis
.
Plant Cell Environ.
39
,
50
61
25
Yin
,
X.
and
Struik
,
P.C.
(
2017
)
Simple generalisation of a mesophyll resistance model for various intracellular arrangements of chloroplasts and mitochondria in C3 leaves
.
Photosynth. Res.
132
,
211
220
26
Earles
,
J.M.
,
Théroux-Rancourt
,
G.
,
Roddy
,
A.B.
,
Gilbert
,
M.E.
,
McElrone
,
A.J.
and
Brodersen
,
C.R.
(
2018
)
Beyond porosity: 3D leaf intercellular airspace traits that impact mesophyll conductance
.
Plant Physiol.
178
,
148
162
27
Ubierna
,
N.
,
Cernusak
,
L.A.
,
Holloway-Phillips
,
M.
,
Busch
,
F.A.
,
Cousins
,
A.B.
and
Farquhar
,
G.D.
(
2019
)
Critical review: incorporating the arrangement of mitochondria and chloroplasts into models of photosynthesis and carbon isotope discrimination
.
Photosynth. Res.
141
,
5
31
28
Evans
,
J.R.
,
Kaldenhoff
,
R.
,
Genty
,
B.
and
Terashima
,
I.
(
2009
)
Resistances along the CO2 diffusion pathway inside leaves
.
J. Exp. Bot.
60
,
2235
2248
29
Terashima
,
I.
,
Hanba
,
Y.T.
,
Tholen
,
D.
and
Niinemets
,
Ü
. (
2011
)
Leaf functional anatomy in relation to photosynthesis
.
Plant Physiol.
155
,
108
116
30
Tholen
,
D.
and
Zhu
,
X.G.
(
2011
)
The mechanistic basis of internal conductance: a theoretical analysis of mesophyll cell photosynthesis and CO2 diffusion
.
Plant Physiol.
156
,
90
105
31
Tosens
,
T.
,
Niinemets
,
Ü.
,
Vislap
,
V.
,
Eichelmann
,
H.
and
Castro Díez
,
P.
(
2012
)
Developmental changes in mesophyll diffusion conductance and photosynthetic capacity under different light and water availabilities in Populus tremula: how structure constrains function
.
Plant Cell Environ.
35
,
839
856
32
Flexas
,
J.
,
Cano
,
F.J.
,
Carriquí
,
M.
,
Coopman
,
R.E.
,
Mizokami
,
Y.
,
Tholen,
D.
et al (
2018
) CO2 diffusion inside photosynthetic organs. In
The Leaf: A Platform for Performing Photosynthesis, Advances in Photosynthesis and Respiration
(
Adams
,
W.W.
and
Terashima
I
, eds), pp.
163
208
,
Springer
,
New York
33
Lu
,
Z.
,
Lu
,
J.
,
Pan
,
Y.
,
Lu
,
P.
,
Li
,
X.
,
Cong
,
R.
et al (
2016
)
Anatomical variation of mesophyll conductance under potassium deficiency has a vital role in determining leaf photosynthesis
.
Plant Cell Environ.
39
,
2428
2439
34
Tholen
,
D.
,
Boom
,
C.
,
Noguchi
,
K.
,
Ueda
,
S.
,
Katase
,
T.
and
Terashima
,
I.
(
2008
)
The chloroplast avoidance response decreases internal conductance to CO2 diffusion in Arabidopsis thaliana leaves
.
Plant Cell Environ.
31
,
1688
1700
35
Tomás
,
M.
,
Flexas
,
J.
,
Copolovici
,
L.
,
Galmés
,
J.
,
Hallik
,
L.
,
Medrano
,
H.
et al (
2013
)
Importance of leaf anatomy in determining mesophyll diffusion conductance to CO2 across species: quantitative limitations and scaling up by models
.
J. Exp. Bot.
64
,
2269
2281
36
Carriquí
,
M.
,
Cabrera
,
H.M.
,
Conesa
,
M.
,
Coopman
,
R.E.
,
Douthe
,
C.
,
Gago
,
J.
et al (
2015
)
Diffusional limitations explain the lower photosynthetic capacity of ferns as compared with angiosperms in a common garden study
.
Plant Cell Environ.
38
,
448
460
37
Tosens
,
T.
,
Nishida
,
K.
,
Gago
,
J.
,
Coopman
,
R.E.
,
Cabrera
,
H.M.
,
Carriquí
,
M.
et al (
2016
)
The photosynthetic capacity in 35 ferns and fern allies: mesophyll CO2 diffusion as a key trait
.
New Phytol.
209
,
1576
1590
38
Carriquí
,
M.
,
Roig-Oliver
,
M.
,
Brodribb
,
T.J.
,
Coopman
,
R.
,
Gill
,
W.
,
Mark
,
K.
et al (
2019
)
Anatomical constraints to nonstomatal diffusion conductance and photosynthesis in lycophytes and bryophytes
.
New Phytol.
222
,
1256
1270
39
Ren
,
T.
,
Weraduwage
,
S.M.
and
Sharkey
,
T.D.
(
2019
)
Prospects for enhancing leaf photosynthetic capacity by manipulating mesophyll cell morphology
.
J. Exp. Bot.
70
,
1153
1165
40
von Caemmerer
,
S.
and
Evans
,
J.R.
(
2015
)
Temperature responses of mesophyll conductance differ greatly between species
.
Plant Cell Environ.
38
,
629
637
41
Xiao
,
Y.
and
Zhu
,
X.G.
(
2017
)
Components of mesophyll resistance and their environmental responses: a theoretical modelling analysis
.
Plant Cell Environ.
40
,
2729
2742
42
Tosens
,
T.
and
Laanisto
,
L.
(
2018
)
Mesophyll conductance and accurate photosynthetic carbon gain calculations
.
J. Exp. Bot.
69
,
5315
5318
43
Veromann-Jürgenson
,
L.L.
,
Tosens
,
T.
,
Laanisto
,
L.
and
Niinemets
,
Ü
. (
2017
)
Extremely thick cell walls and low mesophyll conductance: welcome to the world of ancient living!
.
J. Exp. Bot.
68
,
1639
1653
44
Weissbach
,
A.
,
Horecker
,
B.L.
and
Hurwitz
,
J.
(
1956
)
Enzymatic formation of phosphoglyceric acid from ribulose diphosphate and carbon dioxide
.
J. Biol. Chem.
218
,
795
810
PMID:
[PubMed]
45
Han
,
J.M.
,
Zhang
,
W.F.
,
Xiong
,
D.L.
,
Flexas
,
J.
and
Zhang
,
Y.L.
(
2017
)
Mesophyll conductance and its limiting factors in plant leaves
.
Chin. J. Plant Ecol.
41
,
914
924
46
Slaton
,
M.R.
and
Smith
,
W.K.
(
2002
)
Mesophyll architecture and cell exposure to intercellular air space in alpine, desert, and forest species
.
Int. J. Plant Sci.
163
,
937
948
47
Earles
,
J.M.
,
Buckley
,
T.N.
,
Brodersen
,
C.R.
,
Busch
,
F.A.
,
Cano
,
F.J.
,
Choat
,
B.
et al (
2019
)
Embracing 3D complexity in leaf carbon–water exchange
.
Trends Plant Sci.
24
,
15
24
48
Tcherkez
,
G.
,
Boex-Fontvieille
,
E.
,
Mahé
,
A.
and
Hodges
,
M.
(
2012
)
Respiratory carbon fluxes in leaves
.
Curr. Opin. Plant Biol.
15
,
308
314
49
Flexas
,
J.
,
Díaz-Espejo
,
A.
,
Galmés
,
J.
,
Kaldenhoff
,
R.
,
Medrano
,
H.
and
Ribas-Carbó
,
M.
(
2007
)
Rapid variations of mesophyll conductance in response to changes in CO2 concentration around leaves
.
Plant Cell Environ.
30
,
1284
1298
50
Tazoe
,
Y.
,
von Caemmerer
,
S.
,
Badger
,
M.R.
and
Evans
,
J.R.
(
2009
)
Light and CO2 do not affect the mesophyll conductance to CO2 diffusion in wheat leaves
.
J. Exp. Bot.
60
,
2291
2301
51
Vrábl
,
D.
,
Vašková
,
M.
,
Hronková
,
M.
,
Flexas
,
J.
and
ŠantrČek
,
J.
(
2009
)
Mesophyll conductance to CO2 transport estimated by two independent methods: effect of variable CO2 concentration and abscisic acid
.
J. Exp. Bot.
60
,
2315
2323
52
Douthe
,
C.
,
Dreyer
,
E.
,
Brendel
,
O.
and
Warren
,
C.R.
(
2012
)
Is mesophyll conductance to CO2 in leaves of three Eucalyptus species sensitive to short-term changes of irradiance under ambient as well as low O2?
Funct. Plant Biol.
39
,
435
448
53
Xiong
,
D.
,
Liu
,
X.
,
Liu
,
L.
,
Douthe
,
C.
,
Li
,
Y.
,
Peng
,
S.
et al (
2015
)
Rapid responses of mesophyll conductance to changes of CO2 concentration, temperature and irradiance are affected by N supplements in rice
.
Plant Cell Environ.
38
,
2541
2550
54
Douthe
,
C.
,
Dreyer
,
E.
,
Epron
,
D.
and
Warren
,
C.R.
(
2011
)
Mesophyll conductance to CO2, assessed from online TDL-AS records of 13CO2 discrimination, displays small but significant short-term responses to CO2 and irradiance in Eucalyptus seedlings
.
J. Exp. Bot.
62
,
5335
5346
55
Bernacchi
,
C.J.
,
Portis
,
A.R.
,
Nakano
,
H.
,
von Caemmerer
,
S.
and
Long
,
S.P.
(
2002
)
Temperature response of mesophyll conductance. Implications for the determination of Rubisco enzyme kinetics and for limitations to photosynthesis in vivo
.
Plant Physiol.
130
,
1992
1998
56
Warren
,
C.R.
and
Dreyer
,
E.
(
2006
)
Temperature response of photosynthesis and internal conductance to CO2: results from two independent approaches
.
J. Exp. Bot.
57
,
3057
3067
57
Yamori
,
W.
,
Noguchi
,
K.
,
Hanba
,
Y.T.
and
Terashima
,
I.
(
2006
)
Effects of internal conductance on the temperature dependence of the photosynthetic rate in spinach leaves from contrasting growth temperatures
.
Plant Cell Physiol.
47
,
1069
1080
58
Xiong
,
D.
and
Nadal
,
M.
(
2019
)
Linking water relations and hydraulics with photosynthesis
.
Plant J.
59
Shrestha
,
A.
,
Song
,
X.
and
Barbour
,
M.M.
(
2019
)
The temperature response of mesophyll conductance, and its component conductances, varies between species and genotypes
.
Photosynth. Res.
141
,
65
82
60
Flexas
,
J.
,
Bota
,
J.
,
Escalona
,
J.M.
,
Sampol
,
B.
and
Medrano
,
H.
(
2002
)
Effects of drought on photosynthesis in grapevines under field conditions: an evaluation of stomatal and mesophyll limitations
.
Funct. Plant Biol.
29
,
461
471
61
Flexas
,
J.
,
Barón
,
M.
,
Bota
,
J.
,
Ducruet
,
J.M.
,
Gallé
,
A.
,
Galmés
,
J.
et al (
2009
)
Photosynthesis limitations during water stress acclimation and recovery in the drought-adapted Vitis hybrid Richter-110 (V. berlandieri×V. rupestris)
.
J. Exp. Bot.
60
,
2361
2377
62
Nadal
,
M.
and
Flexas
,
J.
(
2018
) Mesophyll conductance to CO2 diffusion: effects of drought and opportunities for improvement. In
Water Scarcity and Sustainable Agriculture in Semiarid Environment
(
García-Tejero
,
I.F.
and
Durán-Zuazo
VH
, eds), pp.
404
438
,
Elsevier Inc
,
Cambridge
63
Delfine
,
S.
,
Alvino
,
A.
,
Zacchini
,
M.
and
Loreto
,
F.
(
1998
)
Consequences of salt stress on conductance to CO2 diffusion, Rubisco characteristics and anatomy of spinach leaves
.
Aust. J. Plant Physiol.
25
,
395
402
64
Loreto
,
F.
and
Centritto
,
M.C.K.
(
2003
)
Photosynthetic limitations in olive cultivars with different sensitivity to salt stress
.
Plant Cell Environ.
26
,
95
601
65
Volpe
,
V.
,
Manzoni
,
S.
,
Marani
,
M.
and
Katul
,
G.
(
2011
)
Leaf conductance and carbon gain under salt-stressed conditions
.
J. Geophys. Res. Biogeosciences.
116
,
G4
66
Tomás
,
M.
,
Medrano
,
H.
,
Brugnoli
,
E.
,
Escalona
,
J.M.
,
Martorell
,
S.
,
Pou
,
A.
et al (
2014
)
Variability of mesophyll conductance in grapevine cultivars under water stress conditions in relation to leaf anatomy and water use efficiency
.
Aust. J. Grape Wine Res.
20
,
272
280
67
Gu
,
L.
and
Sun
,
Y.
(
2014
)
Artefactual responses of mesophyll conductance to CO2 and irradiance estimated with the variable J and online isotope discrimination methods
.
Plant Cell Environ.
37
,
1231
1249
68
Théroux-Rancourt
,
G.
and
Gilbert
,
M.E.
(
2017
)
The light response of mesophyll conductance is controlled by structure across leaf profiles
.
Plant Cell Environ.
40
,
726
740
69
Terashima
,
I.
,
Miyazawa
,
S.I.
and
Hanba
,
Y.T.
(
2001
)
Why are sun leaves thicker than shade leaves? - Consideration based on analyses of CO2 diffusion in the leaf
.
J. Plant Res.
114
,
93
105
70
Hanba
,
Y.T.
,
Kogami
,
H.
and
Terashima
,
I.
(
2002
)
The effect of growth irradiance on leaf anatomy and photosynthesis in Acer species differing in light demand
.
Plant Cell Environ.
25
,
1021
1030
71
Zhu
,
C.
,
Ziska
,
L.
,
Zhu
,
J.
,
Zeng
,
Q.
,
Xie
,
Z.
,
Tang
,
H.
et al (
2012
)
The temporal and species dynamics of photosynthetic acclimation in flag leaves of rice (Oryza sativa) and wheat (Triticum aestivum) under elevated carbon dioxide
.
Physiol. Plant.
145
,
395
405
72
Sáez
,
P.L.
,
Galmés
,
J.
,
Ramírez
,
C.F.
,
Poblete
,
L.
,
Rivera
,
B.K.
,
Cavieres
,
L.A.
et al (
2018
)
Mesophyll conductance to CO2 is the most significant limitation to photosynthesis at different temperatures and water availabilities in Antarctic vascular species
.
Environ. Exp. Bot.
156
,
279
287
73
Zait
,
Y.
,
Shtein
,
I.
and
Schwartz
,
A.
(
2019
)
Long-term acclimation to drought, salinity and temperature in the thermophilic tree Ziziphus spina-christi: revealing different tradeoffs between mesophyll and stomatal conductance
.
Tree Physiol.
39
,
701
716
74
Pérez-Martín
,
A.
,
Michelazzo
,
C.
,
Torres-Ruiz
,
J.M.
,
Flexas
,
J.
,
Fernández
,
J.E.
,
Sebastiani
,
L.
et al (
2014
)
Regulation of photosynthesis and stomatal and mesophyll conductance under water stress and recovery in olive trees: correlation with gene expression of carbonic anhydrase and aquaporins
.
J. Exp. Bot.
65
,
3143
3156
75
Mizokami
,
Y.
,
Noguchi
,
K.
,
Kojima
,
M.
,
Sakakibara
,
H.
and
Terashima
,
I.
(
2019
)
Effects of instantaneous and growth CO2 levels and abscisic acid on stomatal and mesophyll conductances
.
Plant Cell Environ.
42
,
1257
1269
76
Flexas
,
J.
,
Scoffoni
,
C.
,
Gago
,
J.
and
Sack
,
L.
(
2013
)
Leaf mesophyll conductance and leaf hydraulic conductance: an introduction to their measurement and coordination
.
J. Exp. Bot.
64
,
3965
3981
77
Wang
,
X.
,
Du
,
T.
,
Huang
,
J.
,
Peng
,
S.
and
Xiong
,
D.
(
2018
)
Leaf hydraulic vulnerability triggers the decline in stomatal and mesophyll conductance during drought in rice
.
J. Exp. Bot.
69
,
4033
4045
78
Takezawa
,
D.
,
Komatsu
,
K.
and
Sakata
,
Y.
(
2013
)
ABA as a Universal Plant Hormone
,
Springer-V
,
Berlin Heidelberg
79
Schäufele
,
R.
,
Santrucek
,
J.
and
Schnyder
,
H.
(
2011
)
Dynamic changes of canopy-scale mesophyll conductance to CO2 diffusion of sunflower as affected by CO2 concentration and abscisic acid
.
Plant Cell Environ.
34
,
127
136
80
Rondeau-Mouro
,
C.
,
Defer
,
D.
,
Leboeuf
,
E.
and
Lahaye
,
M.
(
2008
)
Assessment of cell wall porosity in Arabidopsis thaliana by NMR spectroscopy
.
Int. J. Biol. Macromol.
42
,
83
92
81
Houston
,
K.
,
Tucker
,
M.R.
,
Chowdhury
,
J.
,
Shirley
,
N.
and
Little
,
A.
(
2016
)
The plant cell wall: a complex and dynamic structure as revealed by the responses of genes under stress conditions
.
Front. Plant Sci.
7
,
1
18
82
Rui
,
Y.
and
Dinneny
,
J.R.
(
2019
)
A wall with integrity: surveillance and maintenance of the plant cell wall under stress
.
New Phytol.
225
,
1428
1439
83
Gago
,
J.
,
Daloso
,
D.M.
,
Figueroa
,
C.M.
,
Flexas
,
J.
,
Fernie
,
A.R.
and
Nikoloski
,
Z.
(
2016
)
Relationships of leaf net photosynthesis, stomatal conductance, and mesophyll conductance to primary metabolism: a multispecies meta-analysis approach
.
Plant Physiol.
171
,
265
279
84
Ellsworth
,
P.V.
,
Ellsworth
,
P.Z.
,
Koteyeva
,
N.K.
and
Cousins
,
A.B.
(
2018
)
Cell wall properties in Oryza sativa influence mesophyll CO2 conductance
.
New Phytol.
219
,
66
76
85
Clemente-Moreno
,
M.J.
,
Gago
,
J.
,
Díaz-Vivancos
,
P.
,
Bernal
,
A.
,
Miedes
,
E.
,
Bresta
,
P.
et al (
2019
)
The apoplastic antioxidant system and altered cell wall dynamics influence mesophyll conductance and the rate of photosynthesis
.
Plant J.
99
,
1031
1046
86
Burgos
,
A.
,
Szymanski
,
J.
,
Seiwert
,
B.
,
Degenkolbe
,
T.
,
Hannah
,
M.A.
,
Giavalisco
,
P.
et al (
2011
)
Analysis of short-term changes in the Arabidopsis thaliana glycerolipidome in response to temperature and light
.
Plant J.
66
,
656
668
87
Li
,
A.
,
Wang
,
D.
,
Yu
,
B.
,
Yu
,
X.
and
Li
,
W.
(
2014
)
Maintenance or collapse: responses of extraplastidic membrane lipid composition to desiccation in the resurrection plant Paraisometrum mileense
.
PLoS ONE
9
,
e103430
88
Havaux
,
M.
(
1998
)
Carotenoids as membrane stabilizers in chloroplasts
.
Trends Plant Sci.
3
,
147
151
89
Munné-Bosch
,
S.
and
Alegre
,
L.
(
2002
)
The function of tocopherols and tocotrienols in plants
.
Crit. Rev. Plant Sci.
2689
,
31
57
90
Kumar
,
S.V.
,
Taylor
,
G.
,
Hasim
,
S.
,
Collier
,
C.P.
,
Farmer
,
A.T.
,
Campagna
,
S.R.
et al (
2019
)
Loss of carotenoids from membranes of Pantoea sp. YR343 results in altered lipid composition and changes in membrane biophysical properties
.
Biochim. Biophys. Acta Biomembr.
1861
,
1338
1345
91
Lee
,
A.G.
(
2004
)
How lipids affect the activities of integral membrane proteins
.
Biochim. Biophys. Acta Biomembr.
1666
,
62
87
92
Phillips
,
R.
,
Ursell
,
T.
,
Wiggins
,
P.
and
Sens
,
P.
(
2009
)
Emerging roles for lipids in shaping membrane-protein function
.
Nature
459
,
379
385
93
Uehleln
,
N.
,
Lovisolo
,
C.
,
Siefritz
,
F.
and
Kaldenhoff
,
R.
(
2003
)
The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions
.
Nature
425
,
734
737
94
Maurel
,
C.
,
Boursiac
,
Y.
,
Luu
,
D.T.
,
Santoni
,
V.
,
Shahzad
,
Z.
and
Verdoucq
,
L.
(
2015
)
Aquaporins in plants
.
Physiol. Rev.
95
,
1321
1358
95
Hanba
,
Y.T.
,
Shibasaka
,
M.
,
Hayashi
,
Y.
,
Hayakawa
,
T.
,
Kasamo
,
K.
,
Terashima
,
I.
et al (
2004
)
Overexpression of the barley aquaporin HvPIP2;1 increases internal CO2 conductance and CO2 assimilation in the leaves of transgenic rice plants
.
Plant Cell Physiol.
45
,
521
529
96
Flexas
,
J.
,
Ribas-Carbó
,
M.
,
Hanson
,
D.T.
,
Bota
,
J.
,
Otto
,
B.
,
Cifre
,
J.
et al (
2006
)
Tobacco aquaporin NtAQP1 is involved in mesophyll conductance to CO2 in vivo
.
Plant J.
48
,
427
439
97
Uehlein
,
N.
,
Otto
,
B.
,
Hanson
,
D.T.
,
Fischer
,
M.
,
McDowell
,
N.
and
Kaldenhoff
,
R.
(
2008
)
Function of Nicotiana tabacum aquaporins as chloroplast gas pores challenges the concept of membrane CO2 permeability
.
Plant Cell
20
,
648
657
98
Secchi
,
F.
and
Zwieniecki
,
M.A.
(
2013
)
The physiological response of Populus tremula x alba leaves to the down-regulation of pip1 aquaporin gene expression under no water stress
.
Front. Plant Sci.
4
,
507
99
Xu
,
F.
,
Wang
,
K.
,
Yuan
,
W.
,
Xu
,
W.
,
Liu
,
S.
,
Kronzucker
,
H.J.
et al (
2019
)
Overexpression of rice aquaporin OsPIP1;2 improves yield by enhancing mesophyll CO2 conductance and phloem sucrose transport
.
J. Exp. Bot.
70
,
671
681
100
Ogée
,
J.
,
Wingate
,
L.
and
Genty
,
B.
(
2018
)
Estimating mesophyll conductance from measurements of C18OO photosynthetic discrimination and carbonic anhydrase activity
.
Plant Physiol.
178
,
728
752
101
Price
,
G.D.
,
von Caemmerer
,
S.
,
Evans
,
J.R.
,
Yu
,
J.W.
,
Lloyd
,
J.
,
Oja
,
V.
et al (
1994
)
Specific reduction of chloroplast carbonic-anhydrase activity by antisense RNA in transgenic tobacco plants has a minor effect on photosynthetic CO2 assimilation
.
Planta
193
,
331
340
102
Williams
,
T.C.
,
Flanagan
,
L.B.
and
Coleman
,
J.R.
(
1995
)
Photosynthetic gas exchange and discrimination against 13CO, and C18O16O in tobacco plants modified by an antisense construct to have low chloroplastic
.
Plant Phys.
112
,
319
326
103
Gillon
,
J.
and
Yakir
,
D.
(
2001
)
Influence of carbonic anhydrase activity in terrestrial vegetation on the 18O content of atmospheric CO2
.
Science
291
,
2584
2587
104
Momayyezi
,
M.
and
Guy
,
R.D.
(
2017
)
Substantial role for carbonic anhydrase in latitudinal variation in mesophyll conductance of Populus trichocarpa Torr. & Gray
.
Plant Cell Environ.
40
,
138
149
105
DiMario
,
R.J.
,
Quebedeaux
,
J.C.
,
Longstreth
,
D.J.
,
Dassanayake
,
M.
,
Hartman
,
M.M.
and
Moroney
,
J.V.
(
2016
)
The cytoplasmic carbonic anhydrases βCA2 and βCA4 are required for optimal plant growth at low CO2
.
Plant Physiol.
171
,
280
293